Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T01:23:40.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Long-term effects of a maternal high-fat: high-fructose diet on offspring growth and metabolism and impact of maternal taurine supplementation

Published online by Cambridge University Press:  18 November 2019

M. Li ,
C. M. Reynolds ,
C. Gray ,
R. Patel ,
D. M. Sloboda  and
M. H. Vickers Open the ORCID record for M. H. Vickers [Opens in a new window]
M. Li
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
C. M. Reynolds
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
C. Gray
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
R. Patel
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
D. M. Sloboda
Affiliation:
Department of Biochemistry and Biomedical Sciences, Obstetrics and Gynecology and Paediatrics, McMaster University, Hamilton, Canada Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, Canada
M. H. Vickers*
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
*
Address for correspondence: Mark Vickers, Liggins Institute, University of Auckland, 85 Park Road, Grafton, Auckland 1142, New Zealand. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Maternal obesity is associated with obesity and metabolic disorders in offspring. However, there remains a paucity of data on strategies to reverse the effects of maternal obesity on maternal and offspring health. With maternal undernutrition, taurine supplementation improves outcomes in offspring mediated in part via improved glucose–insulin homeostasis. The efficacy of taurine supplementation in the setting of maternal obesity on health and well-being of offspring is unknown. We examined the effects of taurine supplementation on outcomes related to growth and metabolism in offspring in a rat model of maternal obesity.

Design:

Wistar rats were randomised to: 1) control diet during pregnancy and lactation (CON); 2) CON with 1.5% taurine in drinking water (CT); 3) maternal obesogenic diet (MO); or 4) MO with taurine (MOT). Offspring were weaned onto the control diet for the remainder of the study.

Results:

At day 150, offspring body weights and adipose tissue weights were increased in MO groups compared to CON. Adipose tissue weights were reduced in MOT versus MO males but not females. Plasma fasting leptin and insulin were increased in MO offspring groups but were not altered by maternal taurine supplementation. Plasma homocysteine concentrations were reduced in all maternal taurine-supplemented offspring groups. There were significant interactions across maternal diet, taurine supplementation and sex for response to an oral glucose tolerance test , a high-fat dietary preference test and pubertal onset in offspring.

Conclusions:

These results demonstrate that maternal taurine supplementation can partially ameliorate adverse developmental programming effects in offspring in a sex-specific manner.

Keywords

Maternal diethigh fatfructosetaurinenutritional programming
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 4 , August 2020 , pp. 419 - 426
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Worden, JA, Stipanuk, MH. A comparison by species, age and sex of cysteinesulfinate decarboxylase activity and taurine concentration in liver and brain of animals. Comp Biochem Physiol B. 1985; 82, 233–239.CrossRefGoogle ScholarPubMed
Philipps, AF, Holzman, IR, Teng, C, et al.Tissue concentrations of free amino acids in term human placentas. Am J Obstet Gynecol. 1978; 131, 881–887.CrossRefGoogle ScholarPubMed
Schaffer, S, Kim, HW. Effects and mechanisms of taurine as a therapeutic agent. Biomol Ther. 2018; 26, 225–241.CrossRefGoogle ScholarPubMed
Desforges, M, Ditchfield, A, Hirst, CR, et al.Reduced placental taurine transporter (TauT) activity in pregnancies complicated by pre-eclampsia and maternal obesity. Adv Exp Med Biol. 2013; 776, 81–91.CrossRefGoogle ScholarPubMed
Sturman, JA. Taurine in development. J Nutr. 1988; 118, 1169–1176.CrossRefGoogle ScholarPubMed
Desforges, M, Whittaker, H, Farmer, E, et al.Effects of taurine depletion on human placental syncytiotrophoblast renewal and susceptibility to oxidative stress. Adv Exp Med Biol. 2015; 803, 63–73.CrossRefGoogle ScholarPubMed
Tochitani, S. Functions of maternally-derived taurine in fetal and neonatal brain development. Adv Exp Med Biol. 2017; 975, 17–25.CrossRefGoogle ScholarPubMed
Ditchfield, AM, Desforges, M, Mills, TA, et al.Maternal obesity is associated with a reduction in placental taurine transporter activity. Int J Obes (Lond). 2015; 39, 557–564.CrossRefGoogle ScholarPubMed
Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Maternal taurine supplementation attenuates maternal fructose-induced metabolic and inflammatory dysregulation and partially reverses adverse metabolic programming in offspring. J Nutr Biochem. 2015; 26, 267–276.CrossRefGoogle ScholarPubMed
Cherif, H, Reusens, B, Ahn, MT, Hoet, JJ, Remacle, C. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol. 1998; 159, 341–348.CrossRefGoogle ScholarPubMed
Carneiro, EM, Latorraca, MQ, Araujo, E, et al.Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem. 2009; 20, 503–511.CrossRefGoogle ScholarPubMed
Nakaya, Y, Minami, A, Harada, N, et al.Taurine improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous type 2 diabetes. Am J Clin Nutr. 2000; 71, 54–58.CrossRefGoogle Scholar
Boujendar, S, Reusens, B, Merezak, S, et al.Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia 2002; 45, 856–866.CrossRefGoogle ScholarPubMed
Merezak, S, Hardikar, AA, Yajnik, CS, Remacle, C, Reusens, B. Intrauterine low protein diet increases fetal beta-cell sensitivity to NO and IL-1 beta: the protective role of taurine. J Endocrinol. 2001; 171, 299–308.CrossRefGoogle ScholarPubMed
Tang, C, Marchand, K, Lam, L, et al.Maternal taurine supplementation in rats partially prevents the adverse effects of early-life protein deprivation on beta-cell function and insulin sensitivity. Reproduction 2013; 145, 609–620.CrossRefGoogle ScholarPubMed
Ananchaipatana-Auitragoon, P, Ananchaipatana-Auitragoon, Y, Siripornpanich, V, Kotchabhakdi, N. Protective role of taurine in developing offspring affected by maternal alcohol consumption. EXCLI J. 2015; 14, 660–671.Google ScholarPubMed
Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Effects of taurine supplementation on hepatic markers of inflammation and lipid metabolism in mothers and offspring in the setting of maternal obesity. PLoS One 2013; 8, e76961.CrossRefGoogle ScholarPubMed
Rajia, S, Chen, H, Morris, MJ. Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet. J Neuroendocrinol. 2010; 22, 905–914.Google ScholarPubMed
Cardenas-Perez, RE, Fuentes-Mera, L, de la Garza, AL, et al.Maternal overnutrition by hypercaloric diets programs hypothalamic mitochondrial fusion and metabolic dysfunction in rat male offspring. Nutr Metab (Lond). 2018; 15, 38.CrossRefGoogle ScholarPubMed
Korenbrot, CC, Huhtaniemi, IT, Weiner, RI. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod. 1977; 17, 298–303.CrossRefGoogle ScholarPubMed
Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905–915.CrossRefGoogle ScholarPubMed
White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R1464–1472.CrossRefGoogle ScholarPubMed
Murakami, S. The physiological and pathophysiological roles of taurine in adipose tissue in relation to obesity. Life Sci. 2017; 186, 80–86.CrossRefGoogle ScholarPubMed
Wen, C, Li, F, Zhang, L, et al.Taurine is involved in energy metabolism in muscles, adipose tissue, and the liver. Mol Nutr Food Res. 2019; 63, e1800536.CrossRefGoogle ScholarPubMed
Roysommuti, S, Suwanich, A, Lerdweeraphon, W, Thaeomor, A, Jirakulsomchok, D, Wyss, JM. Sex dependent effects of perinatal taurine exposure on the arterial pressure control in adult offspring. Adv Exp Med Biol. 2009; 643, 135–144.CrossRefGoogle ScholarPubMed
Hultman, K, Alexanderson, C, Mannerås, L, et al.Maternal taurine supplementation in the late pregnant rat stimulates postnatal growth and induces obesity and insulin resistance in adult offspring. J Physiol. 2007; 579, 823–833.CrossRefGoogle ScholarPubMed
Roysommuti, S, Thaeomor, A, Khimsuksri, S, Lerdweeraphon, W, Wyss, JM. Perinatal taurine imbalance alters the interplay of renin-angiotensin system and estrogen on glucose-insulin regulation in adult female rats. Adv Exp Med Biol. 2013; 776, 67–80.CrossRefGoogle ScholarPubMed
Ghosh, S, Chowdhury, S, Das, AK, Sil, PC. Taurine ameliorates oxidative stress induced inflammation and ER stress mediated testicular damage in STZ-induced diabetic Wistar rats. Food Chem Toxicol. 2019; 124, 64–80.CrossRefGoogle ScholarPubMed
Connor, KL, Vickers, MH, Beltrand, J, Meaney, MJ, Sloboda, DM. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol. 2012; 590, 2167–2180.CrossRefGoogle ScholarPubMed
Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 2009; 4, e6744.CrossRefGoogle ScholarPubMed
Reynolds, CM, Segovia, SA, Zhang, XD, Gray, C, Vickers, MH. Maternal high-fat diet-induced programing of gut taste receptor and inflammatory gene expression in rat offspring is ameliorated by CLA supplementation. Physiol Rep. 2015; 3, e12588.CrossRefGoogle ScholarPubMed
Reynolds, CM, Segovia, SA, Zhang, XD, Gray, C, Vickers, MH. Conjugated linoleic Acid supplementation during pregnancy and lactation reduces maternal high-fat-diet-induced programming of early-onset puberty and hyperlipidemia in female rat offspring. Biol Reprod. 2015; 92, 40.CrossRefGoogle ScholarPubMed
Feleder, C, Jarry, H, Leonhardt, S, Moguilevsky, JA, Wuttke, W. Evidence to suggest that gonadotropin-releasing hormone inhibits its own secretion by affecting hypothalamic amino acid neurotransmitter release. Neuroendocrinology 1996; 64, 298–304.CrossRefGoogle ScholarPubMed
Gluckman, PD, Lillycrop, KA, Vickers, MH, et al.Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci USA 2007; 104, 12796–12800.CrossRefGoogle ScholarPubMed
Roysommuti, S, Wyss, JM. Perinatal taurine exposure affects adult arterial pressure control. Amino Acids 2014; 46, 57–72.CrossRefGoogle ScholarPubMed
Lerdweeraphon, W, Wyss, JM, Boonmars, T, Roysommuti, S. Perinatal taurine exposure affects adult oxidative stress. Am J Physiol Regul Integr Comp Physiol. 2013; 305, R95–97.CrossRefGoogle ScholarPubMed
Clayton, JA, Collins, FS. Policy: NIH to balance sex in cell and animal studies. Nature 2014; 509, 282–283.CrossRefGoogle ScholarPubMed